Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-25T08:14:05.126Z Has data issue: false hasContentIssue false
  • English
  • Français

NMR studies of ion binding in biological systems

Published online by Cambridge University Press:  17 March 2009

Sture Forsén ,
Torbjörn Drakenberg  and
Håkan Wennerström
Sture Forsén
Affiliation:
Physical Chemistry, Lund University, S-221 00 Lund, Sweden
Torbjörn Drakenberg
Affiliation:
Physical Chemistry, Lund University, S-221 00 Lund, Sweden
Håkan Wennerström
Affiliation:
Physical Chemistry, Chemical Centre, P.O. Box 124
Get access Rights & Permissions [Opens in a new window]

Extract

Biological systems must have evolved in an interplay between a great many organic and inorganic compounds. As a result a considerable number of elements - estimates range between 25 and 30 - are essential for higher life forms such as animals and man (Underwood, 1977; Williams, 1983, 1984).

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 19 , Issue 1-2 , February 1987 , pp. 83 - 114
Copyright
Copyright © Cambridge University Press 1987

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abragam, A. (1961). The Principle of Nuclear Magnetism. London: Oxford University Press.Google Scholar
Andersson, T., Ångström, J., Falk, K. E.. & Forsén, S. (1980). Perchlorate binding to cytochrome c. A magnetic and optical study. Eur. J. Biochem. 110, 363–369.CrossRefGoogle ScholarPubMed
Andersson, A., Drakenberg, T. & Forsén, S. (1985). The interaction of various drugs with calmodulin as monitored by 113Cd NMR. In Caltnodulin Antagonists and Cellular Physiology (ed. Hidaka, H and Hartshorn, D. J.). New York: Academic Press.Google Scholar
Andersson, T., Drakenberg, T., Forsén, S. & Thulin, E. (1981 a). A 43Ca and 25Mg NMR study of rabbit skeletal muscle troponin C. Exchange rates and binding constants. FEBS Lett. 125, 30–43.CrossRefGoogle ScholarPubMed
Andersson, T., Drakenberg, T., Forsén, S., Thulin, E. & Sward, M. (1982). Direct observation of the 43Ca NMR signal from Ca2+ ions bound to proteins. J. Am. chem. Soc. 104, 576–580.CrossRefGoogle Scholar
Andersson, T., Drakenberg, T. Forsén, S., Wieloch, T. & Lindström, M. (1981 b). Calcium binding to porcine pancreatic phospholipase A2 studied by 43Ca NMR. FEBS Lett. 123, 115–119.CrossRefGoogle Scholar
Andersson, A., Forsén, S., Thulin, E. & Vogel, H. J.. (1983). Cadmium–113 nuclear magnetic resonance studies of proteolytic fragments of calmodulin: assignment of strong and weak cation binding sites. Biochemistry 22, 2309–2313.CrossRefGoogle ScholarPubMed
Andersson, T., Thulin, E. & Forsén, S. (1979). Ion binding to cytochrome c. studied by nuclear magnetic quadrupole relaxation. Biochemistry 18, 2487–2493.CrossRefGoogle ScholarPubMed
Armitage, I. M., Pajer, R. T., Schoot Uiterkamp, A. J. M., Chlebowski, J. F. & Coleman, J. E. (1976). Cadmium-113 Fourier transform nuclear magnetic resonance of cadmium(II) carbonic anhydrases and cadmium(II) alkaline phosphotase. J. Am. chem. Soc. 98, 5710–5712.CrossRefGoogle Scholar
Armitage, I. M., Otvos, J. D., Briggs, R. W. & Boulanger, Y. (1982). Structure elucidation of the metal binding sites in metallothionein by 113Cd NMR. Fedn Proc. Fedn Am. socs exp. Biol. 41, 2974–2980.Google Scholar
Armitage, I. M., Schoot Uiterkamp, A. J. M., Chlebowski, J. F. & Coleman, J. E. (1978). 113Cd NMR as a probe of the active sites of metalloenzymes. J. magn. Reson. 29, 375–392.Google Scholar
Babu, Y. S., Sack, J. S., Greenhough, T. G., Bugg, C. E., Means, A. R. & Cook, W. J. (1986). Three-dimensional structure of calmodulin. Nature 315, 37–40.CrossRefGoogle Scholar
Bailey, D. B., Ellis, P. D., Cardin, A. D. & Behnke, W. D. (1978). Cadmium-113 nuclear magnetic resonance studies of metalloproteins. I. [113Cd]Concanavalin A: a preliminary investigation. J. Am chem. Soc. 100, 5236–5237.CrossRefGoogle Scholar
Bailey, D. B., Ellis, P. D. & Fee, J. A. (1980). Cadmium-113 nuclear magnetic resonance studies of cadmium-substituted derivatives of bovine superoxide dismutase. Biochemistry 19, 591–596.CrossRefGoogle ScholarPubMed
Balschi, J. A., Cirillo, V. P. & Springer, C. S. Jr., (1982). Direct high-resolution nuclear magnetic resonance studies of cation transport in vivo. Sodium transport in yeast cells. Biophys. J. 38, 323–328.CrossRefGoogle ScholarPubMed
Baltzer, L., Becker, E. D., Averill, B. A., Hutchinson, J. M. & Gansow, O. A. (1984). 57Fe NMR: Relaxation mechanisms and chemical shifts. J. Am. chem. Soc. 106, 2444–2446.CrossRefGoogle Scholar
Baltzer, L., Becker, F. D., Tschudin, R. G. & Gansow, O. A. (1985). 57Fe NMR spectroscopy of heme proteins: chemical shift anisotropy and relaxation parameters of carbonylmyoglobin. J. chem. Soc. chem. Commun. 1040–1041.CrossRefGoogle Scholar
Barber, J. (1980). Membrane surface charges and potentials in relation to photosynthesis. Biochim. biophys. Acta 594, 253–559.CrossRefGoogle ScholarPubMed
Belton, P. S., Cox, I. J. & Harris, R. K. (1985). Experimental sulphur-33 nuclear magnetic resonance spectroscopy. J. chem. Soc. Faraday Trans. 2, 81, 63–67.CrossRefGoogle Scholar
Belton, P. S., Morris, V. J. & Tanner, S. F. (1985). Interaction of group I cations with iota, kappa and lambda carrageenans studied by multinuclear NMR. Int. J. Biol. Macromol. 7, 53–58.CrossRefGoogle Scholar
Berendsen, H. J. C. & Edzes, H. T. (1973). Observation and general interpretation of sodium magnetic resonance in biological material. Ann. N. Y. Acad. Sci. 204, 459–463.CrossRefGoogle ScholarPubMed
Berliner, J. B., Ellis, P. D. & Murakami, K. (1983). Manganese(II) electron spin resonance and cadmium-113 nuclear magnetic resonance evidence for the nature of the calcium binding site in a-lactalbumins. Biochemistry 22, 5061–5063.CrossRefGoogle Scholar
Bobsein, R. B. & Myers, R. J. (1980). 113Cd NMR spectrum of substituted horse liver alcohol dehydrogenase. J. Am. chem. Soc. 102, 2454–2455.CrossRefGoogle Scholar
Bobsein, R. B. & Myers, R. J. (1981). 113Cd NMR in binary and tertiary complexes of cadmium-substituted horse liver alcohol dehydrogenase. J. biol. Chem. 256, 5313–5316.CrossRefGoogle Scholar
Boulanger, Y., Armitage, I. M., Miklossy, K.-A. & Winge, D. R. (1982). 113Cd NMR study of a metallothionein fragment. Evidence for a two-domain structure. J. biol. Chem. 257, 13717–13719.CrossRefGoogle ScholarPubMed
Boulanger, Y., Vinay, P. & Desroches, M. (1985). Measurement of wide range of intracellular sodium concentration in erythrocytes by 23Na nuclear magnetic resonance. Biophys. J. 47, 553–561.CrossRefGoogle ScholarPubMed
Braun, W., Wagner, G., Wörgötter, E., Vasak, M., Kägi, J. H. R. & Wüthrich, K. (1986). Polypeptide fold in the two metal clusters of metallothionein-2 by nuclear magnetic resonance in solution. J. molec. Biol. 187, 125–131.CrossRefGoogle ScholarPubMed
Braunlin, W. H., Andersson, C. F. & Record, M. T. Jr., (1986 b) 23Na NMR investigations of counterion exchange reactions of helical DNA. Biopolymers 25, 205–211.CrossRefGoogle ScholarPubMed
Braunlin, W. H., Drakenberg, T. & Forsén, S. (1985). Metal ion NMR: Application to biological systems. In Current Topics in Bioenergetics, (ed. Lee, C. P.) vol. 14, pp. 97–147. New York: Academic Press.Google Scholar
Braunlin, W. H., Drakenberg, T. & Nordenskiöld, L. (1987). A 43Ca NMR study of calcium(II)-DNA interaction. Biopolymers. (In the press.)CrossRefGoogle Scholar
Braunlin, W. H. & Nordenskiöld, L. (1986). A potassium-39 NMR study of potassium binding to double-helix DNA. Eur. J. Biochem. 142, 133–139.CrossRefGoogle Scholar
Braunlin, W. H., Vogel, H. J., Drakenberg, T. & Bennick, A. (1986 a). A calcium-43 NMR study of calcium binding to an acidic prolin-rich phosphotprotein from human saliva. Biochemistry 25, 584–589.CrossRefGoogle Scholar
Brevard, C. (1983). High resolution multinuclear magnetic resonance: Instrumentation requirements and detection procedures. In The Multinuclear Approach to NMR Spectroscopy (ed. Lambert, J. B. and Riddell, F. G.). Dordrecht: Reidel.Google Scholar
Briggs, R. W. & Armitage, I. M. (1982). Evidence for site-selective metal binding in calf liver metallothionein. J. biol. Chem. 257, 1259–1262.CrossRefGoogle ScholarPubMed
Bull, T. E. (1972). Nuclear magnetic relaxation of spin nuclei involved in chemical exchange. J. magn. Reson. 8, 344–353.Google Scholar
Chiancone, E., Drakenberg, T., Teleman, O. & Forsén, S. (1985). Dynamics and structural properties of the calcium binding site of bovine serine proteases and their zymogens. A multinuclear NMR and stopped flow study. J. molec. Biol. 185, 201–207.CrossRefGoogle ScholarPubMed
Chiancone, E., Norne, J.-E., Forsén, S., Brunori, M. & Antonini, E. (1975). NMR quadrupole relaxation studies of chloride binding to the isolated haemoglobin from trout (Salmo irideus). Biophys. Chem. 3, 56–62.CrossRefGoogle Scholar
Chlebowski, J. F., Armitage, I. M. & Coleman, J. E. (1977). Allosteric interaction between metal ion and phosphate at the active sites of alkaline phosphatase as determined by 31P NMR and 113Cd NMR. J. biol Chem. 252, 7053–7061.CrossRefGoogle Scholar
Chu, S. C., Pike, M. M., Fossel, E. T., Smith, T. W., Balsch, J. A. & Springer, C. S. Jr., (1984). Aqueous shift reagents for high-resolution cationic nuclear magnetic resonance III. Dy(TTHA)3−, Tm(TTHA)3− and Tm(PPP)−. J. magn. Reson. 56, 33–45.Google Scholar
Civan, M. M., Decani, H., Margalit, Y. & Shporer, M. (1983). Observation of sodium-25 in frog skin by NMR. Am. J. Physiol. 245, C213–C214.CrossRefGoogle Scholar
Cope, F. W. (1965). Nuclear magnetic resonance evidence for complexing of sodium ions in muscle. Proc. Natn. Acad. Sci. USA 54, 225–227.CrossRefGoogle ScholarPubMed
Davis, J. H., Jeffrey, K. R., Bloom, M. & Valic, M. I. (1976). Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42, 390–395.CrossRefGoogle Scholar
Dean, P. A. W., Law, A. Y. C., Szymanska, J. A. & Stillman, M. J. (1983). Cadmium binding to metal-free metallothionein: a correlation of UV, CD and 113Cd NMR data and a 113 Cd NMR characterization of the binding sites in the reconstituted protein. Inorg. chim. Acta 78, 275–279.CrossRefGoogle Scholar
Delville, A., Grandjean, J., Laszlo, P., Gerday, C., Brzeska, H. & Drabikowski, W. (1980 b). Sodium-23 nuclear magnetic resonance as an indicator of sodium binding to calmodulin and tryptic fragments, in relation to calcium content. Ear. J. Biochem. 109, 515–522.CrossRefGoogle ScholarPubMed
Delville, A., Grandjean, J., Laszlo, P., Gerday, C., Grabarek, Z. & Drabikowski, W. (1980 a). Sodium-23 nuclear magnetic resonance as an indicator of sodium binding to troponin C and tryptic fragments, in relation to calcium content and attendant conformational changes. Eur J. Biochem. 105, 289–295.CrossRefGoogle ScholarPubMed
Drakenberg, T., Andersson, T., Forsén, S. & Wieloch, T. (1984). Calcium binding to pancreatic phosholipase A2 and its zymogen. A 43Ca NMR study. Biochemistry 23, 2387–2392.CrossRefGoogle Scholar
Drakenberg, T. & Forsén, S. (1983). The alkaline earth metals — biological applications. In The Multinuclear Approach to NMR Spectroscopy (ed. Lambert, J. B. and Riddell, F. G..) Dordrecht: Reidel.Google Scholar
Drakenberg, T., Forsén, S. & Thulin, E. Unpublished results.Google Scholar
Ellis, P. D. (1982). Personal communication.Google Scholar
Ellis, P. D. (1983 a). Cadmium-113 nuclear magnetic resonance spectroscopy in bipionorganic chemistry. A representative spin-½ metal nuclide. In The Multinuclear Approach to NMR Spectroscopy (ed. Lambert, J. B. and Riddell, F. G..) Dordrecht: Reidel.Google Scholar
Ellis, P. D. (1983 b). Cadmium-113 magnetic resonance spectroscopy. Science 221, 1141–1146.CrossRefGoogle ScholarPubMed
Ellis, P. D., Yang, P. P. & Palmer, A. R. (1983). Cadmium-113 NMR spin-lattice relaxation and exchange kinetics in concanavalin A: a double saturation transfer experiment.J. magn. Reson. 52, 254–266.Google Scholar
Engeseth, H. R., McMillan, R. D. & Otvos, J. D. (1984). Comparative Cd-113 nuclear magnetic resonance studies of Cd(II)-substituted blue copper proteins. J. biol. Chem. 259, 4822–4826.CrossRefGoogle ScholarPubMed
Evelhoch, J. L., Bocian, D. F. & Sudmeier, J. L. (1981). Evidence for direct metal nitrogen binding in aromatic solfonamide complexes of cadmium(II)-substituted carbonic anhydrases by cadmium-113 nuclear magnetic resonance. Biochemistry 20, 4951–4954.CrossRefGoogle Scholar
Falke, J. J., Pace, R. J. & Chan, S. I. (1984 b). Chloride binding to the anion transport binding sites of band 3. A 35Cl NMR study. J. biol. Chem. 259, 6472–6475.CrossRefGoogle Scholar
Falke, J. J., Pace, R. J. & Chan, S. I. (1984 b). Direct observation of the transmembrane recruitment of Band 3 transport sites by competitive inhibitors. A 35Cl NMR study. J. biol. Chem. 259, 6481–6484.CrossRefGoogle ScholarPubMed
Farrar, T. C. & Becker, E. D. (1971). Pulse and Fourier Transform NMR. New York: Academic Press.Google Scholar
Forsén, S., Andersson, T., Drakenberg, T., Lilja, H. & Thulin, E. (1983 a). 43Ca and 25Mg in the study of calcium and magnesium binding to regulatory proteins. Period. Biol. (Jugoslaυ) 85, 31–42.Google Scholar
Forsén, S., Andersson, T., Drakenberg, T., Teleman, O., Thulin, E. & Vogel, H. J. (1983 b). 25Mg, 43Ca and 113Cd NMR studies of regulatory calcium binding proteins. In Calcium Binding Proteins 1983 (ed. de Bernard, B. et al. ). Amsterdam: Elsevier North Holland.Google Scholar
Forsén, S., Andersson, T., Drakenberg, T., Thulin, E. & Swärd, M. (1982). Direct observation of the 43Ca NMR signal from Ca2+-ions bound to proteins. Fedn Proc. Fedn Am. Socs exp. Biol. 41, 2981–2986.Google Scholar
Forsén, S. & Lindman, B. (1981). Ion binding in biological systems measured by nuclear magnetic resonance. In Methods of Biochemical Analysis (ed. Glick, D.), vol. 27, New York: Wiley Interscience.CrossRefGoogle Scholar
Fossel, E. T., Sarasua, M. M. & Koehler, K. A. (1985). A lithium-7 NMR investigation of the lithium ion interaction with phosphatidylcholine-phosphatidylglycerol membranes. Observations of calcium and magnesium ion competition. J. magn. Reson. 64. 536–547.Google Scholar
Gerothanassis, I. P. & Lauterwein, J. (1982). An evaluation of various pulse sequences for the suppression of acoustic ringing in oxygen-17 NMR. J. magn. Reson. 66, 32–42.Google Scholar
Gettins, P. & Coleman, J. E. (1982). 113Cd NMR of Cd(II)-substituted Zn(II) metalloenzymes. Fedn Proc. Fedn Am. Socs exp. Biol. 41, 2966–2973.Google ScholarPubMed
Gettins, P. & Coleman, J. E. (1983). 113Cd nuclear magnetic resonance (II) alkaline phosphatases. J. biol. Chem. 258, 396–407.CrossRefGoogle ScholarPubMed
Gettins, P. & Coleman, J. E. (1984 a). 113Cd NMR arsenate binding to Cd(II) alkaline phosphatase. J. biol. Chem. 259, 4987–4991.CrossRefGoogle ScholarPubMed
Gettins, P. & Coleman, J. E. (1984 b). Zn(II)-113Cd(II) and Zn(II)-Mg(II) hybrids of alkaline phosphatase. 31P and 113Cd NMR. J. Biol. Chem. 259, 4991–4997.CrossRefGoogle Scholar
Grandjean, J. & Laszlo, P. (1978). Binding and release of cations by biopolymers: A sodium-23 NMR study of parvalbumin. In Protons and Ions Involved in Fast Dynamic Phenomena (ed. Laszlo, P.). Amsterdam: Elsevier North Holland.Google Scholar
Grandjean, J., Laszlo, P. & Gerday, C. (1977). Sodium binding to parvalbumins studied by 23Na NMR. FEBS Lett. 81, 376–380.CrossRefGoogle Scholar
Grasdalen, H. & Smidsrød, O. (1981). 113Cd NMR in the Sol-Gel states of aqueous carrageenan. Selective site binding of cesium and potassium ions in κ-carrageenam gels. Macromolecules 14, 229–232.CrossRefGoogle Scholar
Gupta, G. K. & Gupta, P. (1982). Direct observation of resolved resonances from intra and extracellular sodium-23 ions in NMR studies of intact cells and tissues using dysprosium(III) dipolyphosphate as paramagnetic shift reagent. J. magn. Reson. 47, 344–354.Google Scholar
Halle, B. & Wennerström, H. (1981). Nearly exponential quadrupole relaxation. A perturbation treatment. J. magn. Reson. 44, 89–100.Google Scholar
Harris, R. K. & Mann, B. E. (1978). NMR and the Periodic Table. London: Academic Press.Google Scholar
Hubbard, P. S. (1970). Non-exponential nuclear magnetic relaxation by quadrupole interactions. J. chem. Phys. 53, 985–988.CrossRefGoogle Scholar
Khan, A., Jönsson, B. & Wennerström, H. (1985). Phase equilibria in mixed sodium and calcium di-2-ethyl-hexylsulfonsuccinate aqueous systems. An illustration of repulsive and attractive double-layer forces. J. phys. Chem. 89, 5180–5184.CrossRefGoogle Scholar
Kingsley-Hickman, P. B., Nelsestuen, G. L. & Ugurbil, K. (1986). 113Cd NMR study of bovine prothrombin fragment I and factor X. Biochemistry 25, 3352–3355.CrossRefGoogle ScholarPubMed
Kretsinger, R. H. (1976). Calcium-binding proteins. Annu. Rev. Biochem. 45, 239–266.CrossRefGoogle ScholarPubMed
Kurland, R., Newton, C., Nir, S. & Papahadjopoulos, D. (1979). Specificity of Na+ binding to phosphatidylserine vesicles from a 23Na NMR relaxation rate study. Biochim. biophys. Acta 551, 137–143.CrossRefGoogle ScholarPubMed
Lee, H. C., Gard, J. K., Brown, T. L. & Oldfield, E. (1985). Iron-57 nuclear magnetic resonance spectroscopic study of carbonmonoxymyo-globin. J. Am. chem. Soc. 107, 4087–4088.CrossRefGoogle Scholar
Lindman, B. & Forsén, S. (1976). Chlorine, Bromine and Iodine NMR. Physico-chemical and Biological Applications, vol. 12 of the series NMR basic properties and progress (ed. Diehl, P., Fluck, E. and Kosfeldt, R.). Berlin: Springer Verlag.CrossRefGoogle Scholar
Lindblom, G., Wennerström, H. C. & Lindman, B. (1971). Ion binding in liquid crystals studied by NMR. II. 35C1 second-order quadrupole interactions. Chem. Phys. Lett. 8, 489–493.CrossRefGoogle Scholar
Linse, S., Drakenberg, T. & Forsén, S. (1986). Mastoparan binding induces a structural change affecting both the N-terminal and C-terminal domains of calmodulin. A 113Cd NMR study. FEBS Lett. 199, 28–32.CrossRefGoogle ScholarPubMed
Martin, S. R., Andersson, A., Bayley, P., Drakenberg, T. & Forsén, S. (1985). Kinetics and calcium dissociation from calmodulin and its fragments reveals a two domain structure. A quin-2 stopped flow fluorescence study. Eur. J. Biochem. 151, 543–549.CrossRefGoogle ScholarPubMed
Martin, S. R., Linse, S., Bayley, P. M. & Forsén, S. (1986). Kinetics of cadmium and terbium dissociation from calmodulin and its tryptic fragments. Eur. J. Biochem. (In the press.)CrossRefGoogle ScholarPubMed
Martins, E. O. & Drakenberg, T. (1982). Cadmium(II), zinc(II) and copper(II) ions binding to bovine serum albumin. A 113Cd NMR study. Inorg. chim. Acta 67, 71–75.CrossRefGoogle Scholar
Minelli, M., Enemark, J. H., Brownlee, R. T. C., O'Connor, M. J. & Wedd, A. G. (1985). The nuclear magnetic resonance properties of chromium, molybdenum and tungsten compounds. Coord. Chem. Rev. 68, 169–178.CrossRefGoogle Scholar
Monoi, H. (1985). Nuclear magnetic resonance of 23Na ions interacting with the gramicidin channels. Biophys. J. 48, 643–662.CrossRefGoogle Scholar
Morishima, I., Kurono, M. & Shiro, Y. (1986). Presence of endogenous calcium ion in horseradish peroxidase. J. biol. Chem. 261, 9391–9399.CrossRefGoogle ScholarPubMed
Nicholson, J. K., Sadler, P. J., Cain, K., Holt, D. E., Webb, M. & Hawkes, G. E. (1983). 88 MHz 113Cd NMR studies of native rat liver metallothioneins. Biochem. J. 211, 251–255.CrossRefGoogle ScholarPubMed
Nilsson, L. G., Nordenskiöld, L., Stilbs, P. & Braunlin, W. H. (1986). Macroscopic counterion diffusion in solutions of cylindrical polyelectrolytes. J. phys. Chem. 89, 3385–3391.CrossRefGoogle Scholar
Norton, I. T., Morris, E. R. & Rees, D. A. (1984). Lyotropic effects of simple anions on the conformation and interactions of kappa-carrageenan. Carbohydr. Res. 134, 89–93.CrossRefGoogle Scholar
Nozawa, T., Sato, M., Hatano, M., Kobayashi, M. & Osa, T. (1983). 57Fe NMR of iron(II) low spin hemes. Chem. Lett. 1289–1292.CrossRefGoogle Scholar
Oldfield, E. & Skarjune, R. P. (1978). Spin-echo and spin-lock natural-abundance carbon-13 Fourier transform NMR of proteins using a sideways spinning 20-mm tube probe. J. magn. Reson. 31, 527–532.Google Scholar
Otvos, J. D. & Armitage, I. M. (1979). 113Cd NMR of metallothionein: Direct evidence for the existence of polynuclear metal binding sites. J. Am. chem. Soc. 101, 7734–7736.CrossRefGoogle Scholar
Otvos, J. D. & Armitage, I. M. (1980 a). Structure of the metal clusters in rabbit liver metallothionein. Proc. Natn. Acad. Sci. USA 77, 7094–7098.CrossRefGoogle ScholarPubMed
Otvos, J. D. & Armitage, I. M. (1980 b). Determination by cadmium-113 nuclear magnetic resonance of the structural basis for metal ion dependent anticooperativity in alkaline phosphatase. Biochemistry 19, 4031–4043.CrossRefGoogle ScholarPubMed
Otvos, J. D. & Armitage, I. M. (1981). In Biological Structure Determination by NMR (ed. Sykes, B. D., Glickson, J. and Bothner-By, A. A.). New York: Dekker.Google Scholar
Otvos, J. D.Olofson, R. W. & Armitage, I. M. (1982). Structure of an invertebrate metallothionein from Scylla serrata. J. biol. Chem. 257, 2427–2431.CrossRefGoogle ScholarPubMed
Palmer, A. R., Bailey, D. B., Behnke, W. D., Cardin, A. D., Yang, P. P. & Ellis, P. D. (1980). Cadmium-113 nuclear magnetic resonance investigation of metal binding sites in concanavalin A. Biochemistry 19, 5063–5070.CrossRefGoogle ScholarPubMed
Persson, N.-O., Lindblom, G., Lindman, B. & Arvidsson, G. (1974). Deuterium and sodium-23 NMR studies of lecithin mesophases. Chem. Phys. Lipids 12, 261–267.CrossRefGoogle ScholarPubMed
Pettegrew, J. W., Glonek, T., Minshew, N. J. & Woessner, D. E. (1985). Sodium-23 NMR of intact bovine lens and vitreous humor. J. magn. Reson. 63, 439–448.Google Scholar
Pike, M. M., Frazer, J. C., Dedrick, D. F., Ingwall, J. S., Allen, P. D., Springer, C. S. Jr., & Smith, T. W. (1985). 23Na and 39K nuclear magnetic resonance studies of perfused rat hearts. Discrimination of intra- and extra-cellular ions using a shift reagent. Biophys. J. 48, 159–173.CrossRefGoogle Scholar
Pike, M. M., Simon, S. R., Balshi, J. A. & Springer, C. S. Jr., (1982). High-resolution NMR studies of transmembrane cation transport: use of an aqueous shift reagent for 23Na Proc. Natn. Acad. Sci. USA 79, 810–813.CrossRefGoogle ScholarPubMed
Pike, M. M. & Springer, C. S. Jr., (1982). Aqueous shift reagents for high-resolution cationic nuclear magnetic resonance. J. magn. Reson. 46, 348–353.Google Scholar
Potter, J. D. & Gergeley, J. (1975). The calcium and magnesium binding sites on troponin and their role in the regulation of myotibrillar adenosine triphosphatase. J. biol. Chem. 250, 4628–4637.CrossRefGoogle ScholarPubMed
Prigodich, R. V., O'Connor, T. & Coleman, J. E. (1985). 1H, 113Cd and 31P NMR of osteocalcin (bovine γ-carboxy-glutamic acid containing protein). Biochemistry 24, 6291–6298.CrossRefGoogle Scholar
Rose, D. M., Polnaszek, C. F. & Bryant, R. G. (1982). 25Mg NMR investigations of the magnesium ion-DNA interaction. Biopolymers 21, 653–664.CrossRefGoogle ScholarPubMed
Sadler, P. J., Bakka, A. & Beynon, P. J. (1978). 113Cd nuclear magnetic resonance of metallothionein. Non-equivalent CdS4 sites. FEBS Lett. 94, 315–318.CrossRefGoogle ScholarPubMed
Schoot Uiterkamp, A. J. M., Armitage, I. M. & Coleman, J. E. (1980). 113Cd nuclear magnetic resonance of mammalian erythrocyte carbonic anhydrases. J. biol. Chem. 255, 3911–3917.CrossRefGoogle Scholar
Shimizu, T. & Hatano, M. (1985). Magnetic resonance studies of trifluoroperazinecalmodulin solutions: 43Ca, 25Mg, 67Zn and 39K nuclear magnetic resonance. Inorg. Chem. 24, 2003–2009.CrossRefGoogle Scholar
Shporer, M. & Civan, M. M. (1972). Nuclear magnetic resonance of sodium-23 linoleate-water. Basis for an alternative interpretation of sodium-23 spectra with cells. Biophys. J. 12, 114–118.CrossRefGoogle ScholarPubMed
Söderman, O., Arvidsson, G., Lindblom, G. & Fontell, K. (1983). The interaction between monovalent ions and phosphatidyl cholines in aqueous bilayers. Eur. J. Biochem. 134, 309–313.CrossRefGoogle ScholarPubMed
Söderman, O., Engström, S. & Wennerström, H. (1980). Alkali counterion binding specifically in lamellar liquid crystals. J. Colloid Interface Sci. 78, 110–118.CrossRefGoogle Scholar
Sudmeier, J. L. & Bell, S. J. (1977). Cadmium-113 nuclear magnetic resonance studies of 113Cd(II)-substituted human carbonic anhydrase B. J. Am. chem. Soc. 99, 4499–4500.CrossRefGoogle ScholarPubMed
Sudmeier, J. L., Bell, S. J., Storm, M. C. & Dunn, M. F. (1980). Cadmium-113 nuclear magnetic resonance studies of bovine insulin: two-zinc insulin hexamer specifically binds calcium. Science 212, 560–562.CrossRefGoogle Scholar
Sunderalingam, M., Bergstrom, R., Strasburg, G., Rao, S. T., Raychowdhury, P., Grenser, M. L. & Wang, B. C. (1986). Molecular structure of troponin C from chicken skeletal muscle at 3 Ångström resolution. Science 227, 945–948.CrossRefGoogle Scholar
Svärd, M., Drakenberg, T., Andersson, T. & Fernlund, P. (1986). Calcium binding to bone γ-carboxyglutamic acid protein from calf studied by 43Ca NMR. Eur. J. Biochem. 158, 373–378.CrossRefGoogle Scholar
Szebenyi, D. M. E. & Moffat, L. (1986). The refined structure of vitamin D-dependent calcium-binding protein from bovine intestine. Molecular details, ion binding and implications for the structure of other calcium-binding proteins. J. biol. Chem. 261, 8761–8777.CrossRefGoogle ScholarPubMed
Teleman, A., Drakenberg, T. & Forsén, S. (1986). Kinetics of Ca2+ binding to calmodulin and its tryptic fragments studied by 43Ca NMR. Biochim. biophys. Acta 873, 204–213.CrossRefGoogle ScholarPubMed
Thulin, E., Andersson, A., Drakenberg, T., Forsén, S. & Vogel, H. J. (1984). Metal ion and drug binding to proteolytic fragments of calmodulin: Proteolytic, cadmium-113 and proton nuclear magnetic resonance studies. Biochemistry 23, 1862–1870.CrossRefGoogle ScholarPubMed
Tsai, M.-D., Drakenberg, T., Thulin, E. & Forsén, S. (1987). Is the binding of magnesium(II) to calmodulin significant? An investigation by magnesium-25 nuclear magnetic resonance. Biochemistry. (In the press).CrossRefGoogle ScholarPubMed
Underwood, E. J. (1977). Trace Elements in Human and Animal Nutrition, 4th edn.New York: Academic Press.Google Scholar
Urry, D. W., Trapone, T. L., Brown, R. A., Venkatachalam, C. M. & Prassa, K. U. (1985). Cesium-133 NMR longitudinal relaxation study of ion binding to gramicidin transmembrane channel. J. magn. Reson. 65, 43–52.Google Scholar
Vasak, M., Hawkes, G. E., Nicholson, J. K. & Sadler, P. J. (1985). 113Cd NMR studies of reconstituted seven-cadmium metallothionein: evidence for structural flexibility. Biochemistry 24, 740–747.CrossRefGoogle ScholarPubMed
Venkatachalam, C. M. & Urry, D. W. (1980). Analysis of multisite ion binding using sodium-23 NMR with application to channel-forming micellar-packed malonyl gramicidin. J. magn. Reson. 41, 313–317.Google Scholar
Vogel, H. J., Andersson, T., Braunlin, W. H., Drakenberg, T. & Forsén, S. (1984). Trifluoperazine binding to calmodulin. A shift reagent 43Ca NMR study. Biochim. Biophys. Res: Commun. 122, 1350–1356.CrossRefGoogle ScholarPubMed
Vogel, H. J. & Braunlin, W. H. (1985). Shift reagents for calcium-43 NMR studies of calcium-binding proteins. J. magn. Reson. 62, 42–53.Google Scholar
Vogel, H. J., Drakenberg, T. & Forsén, S. (1983). Calcium binding proteins. In NMR of Newly Accessible Nuclei, vol. 2 (ed. Laszlo, P.). New York: Academic Press.Google Scholar
Vogel, H. J., Drakenberg, T., Forsén, S., O'Neill, J. D. J. & Hofmann, T. (1985). Structural differences in the calcium binding sites of the porcine intestinal calcium binding protein, a multinuclear NMR study. Biochemistry 24, 3870–3876.CrossRefGoogle ScholarPubMed
Wang, C.-L. A., Leavis, P. C. & Gergely, J. (1984). Kinetic studies show that Ca2+ and Tb3 have different binding preferences towards the four Ca2+ -binding sites of calmodulin. Biochemistry 23, 6410–6415.CrossRefGoogle Scholar
Welsch, K. M., Armitage, I. M. & Cooperman, B. S. (1983). Yeast inorganic pyrophosphatase. Functional and 113Cd and 31P nuclear magnetic resonance studies of the Cd2+ -enzyme. Biochemistry 22, 1046–1054.CrossRefGoogle Scholar
Welsch, K. M. & Cooperman, B. S. (1984). Yeast inorganic pyrophosphatase. A model for active-site structure based on 113Cd and 31P NMR studies. Biochemistry 23, 4947–4955.CrossRefGoogle Scholar
Wennerström, H., Lindman, B., Lindblom, G. & Tiddy, G. J. T. (1979). Ion condensation model and nuclear magnetic resonance studies of counterion binding in lyotropic liquid crystals. J. chem. Soc. Faraday Trans. I, 75, 663–669.CrossRefGoogle Scholar
Werbelow, L. G. & Marshall, A. G. (1981). The NMR of spin- nuclei: the effect of second-order dynamic frequency shifts. J. magn. Reson. 43, 443–448.Google Scholar
Werbelow, L. G. & Pouzard, G. (1981). Quadrupolar relaxation. The multiquantum coherences. J. phys. Chem. 85, 3887–3891.CrossRefGoogle Scholar
Westlund, P. O. & Wennerström, H. (1982). NHR lineshapes of I = and I = nuclei. Chemical exchange effects and dynamic shifts. J. magn. Reson. 50, 451–466.Google Scholar
Williams, R. J. P. (1983). Inorganic elements in biological space and time. Pure appl. Chem. 55, 1089–1100.CrossRefGoogle Scholar
Williams, R. J. P. (1984). The symbiosis of metal and protein function. Eur. J. Biochem. 150, 231–248.CrossRefGoogle Scholar
Wyckoff, H. W., Handshumacher, M., Murthy, K. & Sowadski, J. M. (1983). The three dimensional structure of alkaline phosphatase from E. coli Adv. Enzymol. 55, 453–479.Google Scholar